Proc. R. Soc. B (2008) 275, 955–962

doi:10.1098/rspb.2007.1619

The Anna’s hummingbird chirps with its tail: anew mechanism of sonation in birds

Christopher James Clark* and Teresa J. Feo

Museum of Vertebrate Zoology, 3101 VLSB, University of California, Berkeley, Berkeley, CA 94720, USA

Published online 29 January 2008

Electron1098/rsp

*Autho

ReceivedAccepted

A diverse array of birds apparently make mechanical sounds (called sonations) with their feathers. Few

studies have established that these sounds are non-vocal, and the mechanics of how these sounds are

produced remains poorly studied. The loud, high-frequency chirp emitted by a male Anna’s hummingbird

(Calypte anna) during his display dive is a debated example. Production of the sound was originally

attributed to the tail, but a more recent study argued that the sound is vocal. Here, we use high-speed video

of diving birds, experimental manipulations on wild birds and laboratory experiments on individual

feathers to show that the dive sound is made by tail feathers. High-speed video shows that fluttering of the

trailing vane of the outermost tail feathers produces the sound. The mechanism is not a whistle, and we

propose a flag model to explain the feather’s fluttering and accompanying sound. The flag hypothesis

predicts that subtle changes in feather shape will tune the frequency of sound produced by feathers. Many

kinds of birds are reported to create aerodynamic sounds with their wings or tail, and this model may

explain a wide diversity of non-vocal sounds produced by birds.

Keywords: hummingbird; sonation; tail feather; mechanical sound; display; Calypte anna

1. INTRODUCTIONAcoustic communication plays an important role in bird

behaviour, sexual selection (Kroodsma & Byers 1991)

and speciation (Price 1998). While the mechanisms of

bird vocalizations have received considerable attention

(Greenewalt 1968; Fletcher & Tarnopolsky 1999; Suthers

et al. 1999), birds also produce a diversity of mechanical

(non-vocal) sounds that are poorly described. Mechanical

sounds are not created by the syrinx, but by other parts of

the animal such as the wings or tail. They may be

adventitious, produced incidentally and involuntarily as

the part of another behaviour, or sonations (Bostwick &

Prum 2003), in which the sound itself plays a role in

communication. Some mechanical sounds are produced

by physical contact between two structures, such as the

percussive or stridulatory sounds made by the wings of

manakins (Pipridae; Bostwick & Prum 2003, 2005).

Other mechanical sounds are aerodynamic sounds

produced by air flowing over or between a bird’s feathers.

Aerodynamic sounds are created by air interacting with

a solid object. Birds fly at high Reynolds numbers, so a large

portion of the flow around them is turbulent. Turbulent

flow produces sound (Fletcher 1992). Under most flow

regimes, turbulence is random, causing random pressure

fluctuations, resulting in atonal sounds characterized by a

continuous distribution of sound frequencies. As a result,

during flight, all birds, including owls (Kroeger et al. 1972),

produce these atonal whooshing flight sounds.

In addition to these ubiquitous atonal sounds, many

flying birds make tonal flight sounds, including swans

(Carboneras 1992), guans (del Hoyo 1994), doves

ic supplementary material is available at http://dx.doi.org/10.b.2007.1619 or via http://journals.royalsociety.org.

r for correspondence (cclark@berkeley.edu).

21 November 20073 January 2008

955

(Mararchi & Baskett 1994), ducks (Lucas & Stettenheim

1972), snipes (Bahr 1907; Carr-Lewty 1943; Reddig

1978; Sutton 1981), hummingbirds (Aldrich 1938; Miller

1940; Rodgers 1940; Miller & Inouye 1983), nighthawks

(Miller 1925; Cleere 1999), larks (Payne 1973; Bertram

1977) and honeyguides (Gill 2007). Many descriptions of

tonal flight sounds call them whistles, but intend this as a

description of the sound’s tonality (Bostwick 2006),

without specifying an underlying whistle mechanism.

Whistles are produced by purely aerodynamic

mechanisms. Conventional whistles can be created by

either air flowing through a constriction (Fletcher 1992),

such as the sound produced by a tea kettle, or air flowing

through a constriction and impinging on an edge

(Fletcher 1992), as in a referee’s whistle. Both of these

mechanisms operate according to

f ZSt v=d ð1:1Þ

where f is the sound frequency; St is a constant (the

Strouhal number); v is the air velocity; and d is a

characteristic length particular to the specific kind of

whistle (Fletcher 1992). In a third type of whistle, called

an aeolian whistle, the turbulent wake behind a single

object is not entirely random, and vortices form and are

shed at a particular rate, creating a von Karman vortex

street (Fletcher 1992; Vogel 1994). Equation (1.1) still

applies: d is the diameter of the object and the Strouhal

number is approximately 0.2 (Fletcher 1992; Vogel 1994;

White 1999). An example is the sound produced by

telephone wires in high wind (Vogel 1994). According to

these principles, if feathers whistle, it will either be due to

air flowing through a gap between two feathers

(a conventional whistle) or by one feather shedding

vortices at a Strouhal number of approximately 0.2 (an

aeolian whistle), and in either case, the sound frequency

will be proportional to the air velocity.

This journal is q 2008 The Royal Society

spreads tail

Figure 1. A composite image of a male Anna’s hummingbirddiving to a female, created using high-speed video. Consecu-tive images are 0.01 s apart. During the dive, males spreadtheir tails for 0.06 s (nZ5 videos) and simultaneouslyproduce a loud sound (element Cdive in figure 2a) for 0.05 s(nZ53 sound recordings). Videos of two dives are available inthe electronic supplementary material.

956 C. J. Clark & T. J. Feo A new mechanism of sonation in birds

Airflow can also produce tonal sounds if the air excites a

solid to vibrate. Solids have resonant frequencies that are a

function of their stiffness and shape (Blevins 1979). If

moving air excites a feather, it may vibrate at or near its

resonant frequency, producing a tonal sound. This is

qualitatively similar to the reed in a wind instrument

(Fletcher 1992; Fletcher & Rossing 1998). The solid’s

resonant frequency is not affected by air velocity, except by

changes in the air’s added mass (Blevins 1979; Vogel 1994;

Argentina & Mahadevan 2005). Therefore, if feathers

vibrate according to this mechanism, their frequency will

vary little with air velocity.

Studies have used three kinds of evidence to show that a

flight sound is mechanically produced by feathers, rather

than vocally. First, the flight kinematics of many taxa

suggest that their tonal flight sounds are non-vocal. For

instance, the dive sound made by common nighthawks

(Chordeiles minor) only occurs when the wings are turned

down during a stereotypical dive, and this correlation

between behaviour and sound production led Miller

(1925) to conclude that the primary wing feathers create

the dive sound. Second, experimental manipulations can

show that particular feathers are necessary to produce a

flight sound. Miller & Inouye (1983) demonstrated that

gluing shut a gap between two wing feathers, eliminates the

production of a ‘wing whistle’ emitted during flight of

broad-tailed hummingbirds (Selasphorus platycercus).

Third, laboratory experiments can demonstrate that

particular feathers are sufficient to produce sounds similar

to the flight sounds. For instance, isolated snipe tail

feathers placed in moving air create sound similar to the

‘drumming’ noise produced during the species’ charac-

teristic dives (Bahr 1907; Carr-Lewty 1943; Reddig 1978).

In some cases, the origin of a flight sound is debatable

(Bostwick 2006), such as a loud sound produced by male

Anna’s hummingbirds (Calypte anna). During a mating

display, males ascend approximately 30 m in the air before

dropping headfirst and swooping over a female (figure 1;

Hamilton 1965; Stiles 1982). During the dive, a series of

sounds are emitted (figure 2a). The loudest noise is called

element Cdive (Baptista & Matsui 1979) and sounds like a

brief loud chirp or squeak. It is tonal with a fundamental

frequency of 4 kHz and higher harmonics, corresponding

approximately to the musical note C8, four octaves above

Middle C (figure 2a). Males have modified outer tail

feathers, termed rectrix (R5; figure 3a,d ). Rodgers (1940)

reports that he ‘attached an outer tail feather [R5] to a

slender strip of bamboo. By whipping this through the air a

note was produced, which was almost identical with that

produced by the bird.’ Baptista & Matsui (1979) were not

convinced by Rodger’s brief account, and observed that

the Anna’s hummingbird’s song (figure 2b) has elements

Asong, Bsong and Csong that are spectrally and temporally

similar to Adive, Bdive and Cdive. They concluded that the

dive sounds of the Anna’s hummingbird are produced

vocally. Stiles (1982; Stiles et al. 2005) disagrees, arguing

that element Cdive seems louder than the song and too

loud to be produced vocally.

Baptista & Matsui’s (1979) results do not rule out the

possibility that the tail produces element Cdive, and that

acoustic similarity between the song and the dive sound

has arisen via convergent evolution. Here, we show that

element Cdive is a sonation created by fluttering of the

trailing vane (T.V.) of the R5 tail feathers, using three lines

Proc. R. Soc. B (2008)

of evidence: the kinematics of the dive; experiments on

wild birds performing dives; and laboratory experiments

on individual tail feathers.

2. MATERIAL AND METHODS(a) Field experiments

Experiments on live Anna’s hummingbirds were performed at

the ‘Albany Bulb’ portion of the East Shore State Park,

Albany, CA, in spring of 2006 and 2007.

Territorial male Anna’s hummingbirds use a few (less than

10) stereotypical, conspicuous song perches. We located

territorial males, and placed hummingbird feeders on their

territories. Display dives were elicited from individual males

by placing a stuffed mount of an Anna’s hummingbird, or a

live, caged hummingbird in a conspicuous location on a

male’s territory. A Sennheiser ME67 microphone was placed

close to the cage or mount to record dives. Dive sound

recordings were sampled at 48 kHz using a 16 bit digital

recorder (Marantz PMD 670), and saved as uncompressed

WAV files. Sound recordings were visualized using RAVEN v.

1.2.1 (Cornell Lab of Ornithology, Ithaca, NY; Charif et al.

2007) on a PC. Spectrograms were created using a Hann

function with a 512 sample window.

Male Anna’s hummingbirds dive in a vertical plane (the

dive plane) oriented towards the Sun (Hamilton 1965),

allowing us to anticipate the direction in which a bird

would dive. We estimated dive speed by collecting video of

25 dives with digital camcorders (23 dives: 60 fps, 640!480

pixels with a Sony Handicam; 2 dives: 500 fps, 1280!1024

pixels with a Fastec Troubleshooter) placed approximately

20 m from and orthogonal to the dive plane. A metre stick

was held horizontally and vertically in the camera’s image

plane, at the bottom of the display dive (where element Cdive

is produced), as a calibration. Peak Motus (Vicon: Cen-

tennial, CO) was used to digitize the bird’s position over time

in the videos, and to calculate the bird’s instantaneous

velocity using a quintic spline. Accurate estimates of velocity

depend on whether the bird’s dive was really parallel to the

image plane of the camera, and this method will under-

estimate the bird’s true velocity if it was actually diving

somewhat towards or away from the camera. Dives in which

the bird’s motion towards or away from the camera was small

were used to calculate velocity, and none of our conclusions

are affected by an underestimate of the bird’s velocity.

freq

uenc

y (k

Hz)

wav

efor

m

5

10

15

20

0.5 1.0 1.50

5

10

15

20

0.5 1.0 1.50

(a) (b)

Adive Bdive

Cdive

Asong Bsong

Csong

(c) (d ) (e)

AdiveBdive

Cdive

AdiveBdive

freq

uenc

y (k

Hz)

wav

efor

m

seconds

Figure 2. Spectrograms (showing frequency versus time) and waveforms (showing amplitude versus time) of sounds. Greyscale,relative sound energy, in which black indicates high sound energy, and white indicates low sound energy. All five sounds arefrom different recording and therefore their waveforms cannot be directly compared due to different recording conditions.(a) Dive sound from an unmanipulated male, (b) song from a male hovering close to the microphone, (c) dive sound of a malewith no trailing vane (T.V.), (d ) dive sound of a male with no leading vane (L.V.) and (e) is the sound of an R5 feather producingsound in a wind tunnel at an airspeed of 26.2 m sK1. A, B and C are the sound elements of the display dive or song, as defined byBaptista & Matsui (1979). With (a) unmanipulated birds and (d ) birds missing the L.V. of R5, (b) Cdive is present with afundamental frequency of 4 kHz, and is louder than the song. With birds missing the T.V. of R5 (c), Cdive is missing, and insteadthe bird produces a broad-spectrum ‘whoosh’ sound (indicated by the arrow). When R5 is placed in a wind tunnel (e), it producesa sound with a fundamental frequency of 4 kHz that matches a normal Cdive (initiation of sound production indicated by thearrow). The sound recordings used to create these spectrograms are available in the electronic supplementary material.

A new mechanism of sonation in birds C. J. Clark & T. J. Feo 957

Five high-speed videos showing the tail kinematics of

diving birds were also made with a Redlake Motion-

Meter (Kodak; 500 fps, 292!210 pixels) or a Trouble-

shooter (Fastec; 500 fps, 1280!1024 pixels) camera. These

videos were not synchronized with simultaneous sound

recordings.

After pre-manipulation dives were recorded, we captured

males using feeder traps, marked them with small spots of

paint for identification and manipulated one bilateral pair

of tail feathers. Two males had R5 plucked, two had the T.V.

of R5 trimmed off, one had the leading vane (L.V.) of R5

trimmed off three males had R4 plucked and two males had

R3 plucked. After manipulation, males were located on their

territories, and post-manipulation dives were recorded within

Proc. R. Soc. B (2008)

two weeks of manipulation. Plucked feathers regrow in

approximately five weeks.

Comparisons between the loudness of the song and display

dive were obtained from three males. These males perched or

hovered within 1 m of the microphone and sang, facing the

microphone. Immediately prior to or following the song, they

performed normal display dives, passing by at distances greater

than 1 m from the microphone. In addition to differences in

distance, two other factors introduce bias: in one instance the

gain on the recorder was adjusted slightly in favour of the song

seeming louder, and in the other two, the waveforms of the

dive sounds exceeded the recorder’s range of sensitivity. All

three factors bias the songs to seem louder, whereas our

hypothesis is that the dive sound is louder (Stiles 1982).

R1R2

R3R4 R5

(d )

soun

d (k

Hz)

2

3

4

5

2 3 4 5T.V. flutter (kHz)

(b)

leading vane (L.V.)

trailing vane (T.V.)

air flow

4mm

(c)

T.V. flutters up and down

no L.V.

unmanip

no T.V.

base

basetip

L.V.

(e)

shaft

T.V.

(a)

Figure 3. A description of the fluttering of the trailing vane (T.V.) of R5. (a) A male Anna’s hummingbird with tail feathers(rectrices) labelled as R1 through R5. (b) Frequency of the T.V. flutter and that of sound ( f ) are highly correlated (linearregression, unmanipulated feathers: slopeZ0.996, r 2Z0.94, p!0.0001, nZ18); circles, feathers missing L.E.; diamonds,unmanipulated feathers. The correlation between sound production and the T.V. flutter is unaffected by removing the leadingvane (L.V.) of the feather (linear regression, feathers lacking L.V.: slopeZ1.00, r 2Z0.98, p!0.0001, nZ8). (c) Photos of anunmanipulated R5, R5 with the L.V. removed and R5 with the T.V. removed. (d ) An outline of the R5 showing the base, tip,shaft, L.V. and T.V.. (e) Four end-on views showing the up-and-down fluttering motion of the T.V. (in grey), relative to thedirection of airflow. The tip of the feather is not shown in this perspective. Two videos showing the feather fluttering are availablein the electronic supplementary material.

958 C. J. Clark & T. J. Feo A new mechanism of sonation in birds

(b) Laboratory experiments

Tail feathers were collected from wild adult Anna’s humming-

birds caught in Berkeley, CA. We produced sounds using just

the feathers with two methods: by placing them in front of a

jet of air, or by putting them in a wind tunnel.

(i) Jet experiments

Tones were produced by placing the male R5 tail feathers

approximately 2 cm in front of a jet of air issued from a hose.

The outer or L.V. of the feather faced into the jet, and the angle

of attack of the feather was nominally 08 (ignoring aeroelastic

deformation of the feather, which was estimated by eye to be

less than 108 along the entire feather). A Sennheiser ME 67

shotgun microphone was placed next to the jet to record

sound, using the same equipment and settings as the field

experiments. The feather was illuminated using two halogen

lights, and video was collected at 20 000 fps (Photron Fastcam

APX RS, resolution: 512!256 pixels). Sound and video

recordings were manually synchronized to the nearest 1 s.

The jet was made of two lengths of Nalgene premium

tubing (5/16 in. i.d.) each connected to a pressurized air

source. Seven straws (3 mm diameter) were inserted 13 cm

deep into the end of each tube to make the flow more laminar.

This improved the consistency of sounds produced by the

feathers. The ends of the tubes were placed side-by-side to

make a jet that was 2 by 1 cm in cross section. It was large

enough to contain the majority, but not all, of a feather within

the airflow. The use of jets with larger cross-sectional area (that

would contain more of the feather within the airflow) was not

possible due to the higher levels of background noise produced

by them. The speed of the jet was measured with a Kurtz 2440

Proc. R. Soc. B (2008)

thermal anemometer 2 cm from the jet (in the same location as

the feather), and was on average 40 m sK1. It is not clear

whether the turbulence of the jet affected the anemometer’s

accuracy. The value of 40 m sK1 was used solely to ensure

similar aerodynamic conditions across all experiments that

used the jet, at a velocity well above the feather’s critical

velocity. The airflow did not represent aerodynamic conditions

identical to those the feathers experience during a dive, but

tones produced in front of the jet under these conditions

matched the frequencies of sounds produced by feathers

placed in a wind tunnel (see below).

We performed two experimental manipulations: (i) cutting

off the T.V. of the feather (nZ3 feathers) or (ii) cutting off the

L.V. of the feather (nZ3 feathers). To assess changes caused

by experimental manipulations, we placed feathers in the jet

of air perpendicular to airflow, and adjusted their orientation

slightly (if necessary) until they produced sound. Most

unmanipulated male R5 feathers begin producing sounds

immediately when placed in the jet, and if for some reason a

feather did not initially produce sound, manipulating its

orientation for less than 10 s was sufficient to produce a tone.

If an experimentally manipulated feather did not produce

a sound after at least 1 min of adjusting its orientation, it was

scored as not producing sound. Simultaneous sound

recordings and high-speed video (20 000 fps) were taken for

each feather, and it was then removed from the jet. Each

feather was measured three times before manipulation, and

three times after manipulation. We calculated the frequency

of the fluttering motion of the feather by counting the number

of frames necessary for 15 cycles of oscillation.

Table 1. Results of experimental manipulation of feathers R3, R4 and R5 on wild Anna’s hummingbirds. (Italicsindicate manipulations that resulted in a statistically significant change in the proportion of dives with element C present(c2-tests, p!0.002).)

feather manipulationproportion of pre-manipulationdives with element C present result of manipulation N (birds)

pluck R5 100% (nZ20 dives) element C eliminated ( present in 0 of 37 dives) 2remove trailing vane of R5 100% (nZ67 dives) element C eliminated ( present in 0 of 87 dives) 2remove leading vane of R5 100% (nZ9 dives) no difference (13 of 14 dives with element C) 1pluck R4 100% (nZ13 dives) can still produce element C (9 of 18 dives with

element C )3

pluck R3 97.5% (nZ39 dives) no difference (14 of 14 dives with element C) 2

A new mechanism of sonation in birds C. J. Clark & T. J. Feo 959

(ii) Wind tunnel experiments

We placed feathers in a high-speed wind tunnel at the John

Hopkins Marine Research Station, Stanford University, CA.

Feathers were attached to a beam projecting into the working

section of the tunnel, along with a TSI VelociCalc thermal

anemometer placed just upstream and above the feather to

measure the air velocity. Rotating the beam allowed the angle

of attack of the feather to be changed, and the base of the

feather was always perpendicular to the airflow. Audio

recordings were taken with a Sennheiser ME 67 microphone

attached to the outside of the tunnel near the feather. Placing

the microphone inside the tunnel was not possible due to

noise caused by turbulence, and because the microphone’s

windshield blocked roughly 10% of the cross section of the

working section, causing noticeable changes to the tunnel’s

velocity. Attached to the outside of the tunnel, the

microphone was approximately 20 cm from the feather,

with an acrylic barrier (the wall of the working section of

the wind tunnel) between the two. Also, the tunnel motor

produced extremely high levels of background noise. Despite

these constraints, the male R5 produced loud sounds clearly

audible to us outside the wind tunnel, and unambiguously

recorded by the microphone (figure 2e).

The wind tunnel was first set to 26.2 m sK1 and then wind

speed was decreased in increments of 1.6 m sK1 until the

feather ceased producing sound. The presence or absence of

sound production was determined by ear, as, given the

constraints of our setup, the microphone was not more sensitive

than our own hearing. Once the feather stopped producing

sound, the wind velocity was increased in increments of

0.7 m sK1 until the feather once again began to produce a

tone. At each speed, we slowly rotated the angle of attack of the

feather fromK908 to 908; the tone’s frequency varied little with

the angle of the attack, and the feather was rotated to ensure

that it did or did not make sound regardless of its orientation. A

feather’s critical velocity was defined as the minimum velocity

at which it produced audible sound.

3. RESULTSThe high-speed video (500 fps) of males performing

display dives revealed that they began the dive with their

tail shut, then abruptly spread their tail at the bottom of

the dive and held it open for an average of 0.059G0.007 s

(figure 1; nGs.d.; nZ5). Males spread their tails at the

same time element Cdive was produced at the bottom of

the dive. Sound recordings of display dives indicated that

element Cdive lasted for 0.052G0.006 s (nGs.d.; nZ53).

In unmanipulated males, the sound measurements

indicated that element Cdive had a fundamental frequency

Proc. R. Soc. B (2008)

of 4.1G0.2 kHz with harmonics (nZ53; figure 2a);

however the birds travelled 23.1G3.1 m sK1 (nGs.d.

nZ25) at the bottom of the dive, causing further

uncertainty in the sound’s true frequency due to a Doppler

shift of up to G0.3 kHz. Element Cdive was at least 18 dB

louder than any part of the song (paired t-test, pZ0.0005,

d.f.Z2). This was despite three variables (microphone

distance, recorder gain and the recorder’s limited range of

sensitivity) that would bias the song to make it seem

relatively louder (figure 2a,b). Two videos of dives are

available in the electronic supplementary material.

The results of experiments on wild males are sum-

marized in table 1. Experimental manipulation showed

that the T.V. of the R5 tail feathers must be present for the

birds to produce the dive sound. Unmanipulated males

produced element Cdive in 97.3% of dives (nZ402 dives

across 24 birds). All males with R3 or R4 removed

produced element Cdive in at least one of their display

dives. Likewise, a male with the L.V. of R5 removed also

produced element Cdive in most of his dives (figure 2d ).

However, males that had their entire R5 removed, or the

T.V. of R5 removed (figure 3c), never produced element

Cdive after manipulation (table 1; figure 2c). Some sound is

still produced (see vicinity of arrow in figure 2c), but it is a

broad-spectrum sound and generally atonal. Sound files

used to make figure 2 are available in the electronic

supplementary material.

Isolated male R5 feathers made tonal sounds at the

same frequency as element Cdive. Unmanipulated R5

produced tones with fundamental frequencies ranging

from 3.3 to 4.7 kHz, with harmonics, in front of a jet of air

(figure 3b) or in a wind tunnel (figure 2e). R5 feathers with

the L.V. removed (figure 3c) also produced sounds with

frequencies ranging from 2.5 to 4.5 kHz (nZ3 feathers).

However, R5 did not produce sounds after the T.V. was

removed (nZ3 feathers). Male R4 and R3 feathers also

made sounds in a jet of air, at frequencies below 2.5 kHz.

Additionally, male R5 feathers made a second sound that

is associated with the feather’s tip, but at a frequency

below 1.5 kHz.

The high-speed video (20 000 fps) of feathers placed in

the jet revealed that while a feather made a tone, the T.V.

of the feather fluttered at the same frequency as the sound

(figure 3b) while the shaft and L.V. were immobile

(figure 3e). The T.V. of the feather is a sheet of connected

barbs with one edge anchored to the shaft, and free at the

opposite edge (the trailing edge). When the feather

produced sound, the trailing edge of the sheet fluttered

up and down. In most videos, a travelling wave appeared

to move down the feather, either from base to tip or from

0

1

2

3

4

18 20 22 24 26

velocity (ms–1)

freq

uenc

y (k

Hz)

(a)

(b)

Figure 4. Frequency of sound produced by six male R5feathers over a range of air velocities in a wind tunnel.Frequency ( f, kHz) is positively correlated with velocity

(v, m sK1): fZ0.056!vC2.6 (linear regression, slope:p!0.001, intercept: p!0.001, nZ34 samples). Theminimum velocity at which each feather would producesound is circled. (a) The predicted sound frequency for theaeolian whistle hypothesis, according to equation (1.1), and

960 C. J. Clark & T. J. Feo A new mechanism of sonation in birds

tip to base (see videos in the electronic supplementary

material). Sometimes this travelling wave was absent, but

the feather still fluttered and produced the 4 kHz sound.

When the barbs were separated from each other so that

they no longer formed a continuous sheet, the T.V. no

longer fluttered in synchrony, and no sound was detected

above the background noise of the jet. Manually

reconnecting the barbs to reform the sheet enabled the

feather to once again produce audible sound. The

frequency of the sound was almost perfectly correlated

with the frequency of the flutter (regression, slopeZ0.996,

r 2Z0.94, p!0.0001, nZ18; figure 3b). Two high-speed

videos of feathers fluttering in the jet are available in the

electronic supplementary material.

When R5 feathers were placed in a wind tunnel, the

frequency ( f, kHz) of the sound was positively correlated

with air velocity (v, m sK1): ( fZ0.056!vC2.6, linear

regression, slope p!0.001, intercept: p!0.001, nZ34

samples, figure 4). Below a critical minimum velocity of

19.6G1.1 m sK1 (nGs.d., nZ6 birds), the feathers

stopped making audible sounds.

assuming StZ0.2 and dZ4 mm. (b) The birds travel anaverage of 23.1 m sK1 at the bottom of the dive, which isgreater than the average critical velocity of 19.6 m sK1.

4. DISCUSSION

The high-speed video indicates that the Anna’s humming-

bird spreads its tail at the bottom of the display dive

(figure 1). Element Cdive lasts for the same amount of time

as the tail is spread, and occurs at the same part of the dive.

This suggests that spreading the tail plays a role in the

production of the 4 kHz dive sound. Removing R5 or

trimming the T.V. of R5 eliminates element Cdive of the

dive sound in wild birds (figure 2c). These manipulated

birds still produce an atonal sound (figure 2c), but we

hypothesize that this is an adventitious sound made by

turbulent airflow over the body, wings and tail of the bird

as it flies by the microphone. Males with no R3, R4 or a

L.V. of R5 could still generate element Cdive (figure 2d ).

When placed in a jet of air, or in a wind tunnel, the T.V. of

R5 flutters and can produce a 4 kHz sound, at the

velocities reached by male when element Cdive is produced

during a dive (figure 4). Therefore, the T.V. of R5 is both

necessary and sufficient to produce element Cdive. We

conclude that element Cdive is a sonation produced by the

fluttering of the T.V. of the R5 tail feathers.

(a) Acoustic mechanisms

Our data suggest that the mechanism generating element

Cdive is not a whistle. First, morphology rules out the

conventional whistle hypothesis. Conventional whistles

require a gap for air to flow over or through, which would

be created by two feathers or possibly a gap in the barbs of

one feather. Although plucking the R4 feather did

significantly decrease the fraction of dives with element

Cdive present (table 1), suggesting R4 does play a role in

sound production, all three manipulated birds produced

element Cdive at least once when missing their R4s

(table 1), and R5 alone can generate the sound in a wind

tunnel, with no gap present. Thus, the sound is not a

conventional whistle. The Cdive is also not an aeolian

whistle or tone, with tonality produced by vortex shedding

(Fletcher 1992), for four reasons. First, given a Strouhal

number of 0.2 (Vogel 1994; White 1999), a feather width

of 4 mm (figure 3d ) and a velocity of 23 m sK1 at the

bottom of the dive (figure 4), this hypothesis predicts a

Proc. R. Soc. B (2008)

frequency of 1 kHz, not 4 kHz. Second, none of the whistle

hypotheses predict a critical velocity for sound production,

but all of the R5 tail feathers ceased producing sound at

around the same air velocity. Third, although frequency

and velocity are positively correlated (figure 4), the slope is

one-third of that predicted by equation (1.1). Moreover,

the whistle hypothesis predicts that the y-axis intercept

should be near zero, rather than the value of 2.6 kHz

extrapolated from the regression (figure 4). Fourth,

according to the whistle hypothesis, experimental manip-

ulations of the T.V. should change the tone of the sound

(by changing d from equation (1.1)), but not necessarily

eliminate sound production. Instead, manipulations of

the T.V. eliminated the feather’s ability to produce sound.

Our data are consistent with the flag hypothesis, in

which the sound is produced by the feather fluttering at

its resonant frequency. The experiments indicate the T.V.

of the R5 as the source of the sound, suggesting that the

resonance lies within the mechanical properties of the T.V.

of the feather. Reeds in wind instruments (Fletcher &

Rossing 1998) and flags (Argentina & Mahadevan 2005)

represent two structures that vibrate in fluid flow at a

resonant frequency determined by their elastic modulus

and shape.Argentina & Mahadevan (2005) derive equations

predicting that a flag flutters when the airflow exceeds a

critical velocity, and that above this velocity the flutter

frequency is insensitive to wind velocity. The R5 feathers

have a critical minimum velocity for sound production

and therefore a critical velocity for fluttering (figure 4).

Above the critical velocity, the frequency produced by R5

changes little with wind velocity (figure 4). Both of these

results are consistent with Argentina & Mahadevan’s (2005)

model, therefore we fail to reject the flag model as the

mechanism of sound production.

(b) Evolutionary implications

According to the flag model, a feather’s shape and material

properties (i.e. elastic modulus of b-keratin) together set its

pitch, which changes little over a range of air velocities.

A new mechanism of sonation in birds C. J. Clark & T. J. Feo 961

Evolution could theoretically change either shape or elastic

modulus to alter the tone produced by a feather. However,

feather keratin appears to have an invariant elastic modulus

across diverse avian taxa (Bonser & Purslow 1995),

suggesting that flight sounds are not tuned by modifying

this variable. By contrast, feather shape is determined by

variation in barb length, barb diameter and barbule

morphology, which are evolutionarily labile traits (Prum &

Williamson 2001). Therefore, this seems the simplest

pathway for evolution to modify the frequency of flight

sounds produced by feathers. According to this hypothesis,

aspects of feather shape should correlate highly with the

sounds produced by feathers.

A second prediction of the flag model is that feather

tones are only created when airflow over the feather

exceeds a critical velocity. This suggests that tonal flight

sounds will only be associated with behaviours that

produce rapid airflow over the feathers. For sounds

produced by primary wing feathers, birds could attain

sufficient local air velocities to produce sound by varying

their wing-beat kinematics. Mourning doves (Zenaida

macroura) make a tonal sound that appears to be

mechanically produced by the wings (Mararchi & Baskett

1994). This sound is produced primarily during take-off,

which may be due to the high wingtip velocity caused by

take-off kinematics. For other feathers, such as tail

feathers, varying flight speed is the main option available

to modulate local air velocity in order to exceed a feather’s

critical velocity. The Anna’s hummingbird is a case in

point: the behaviour of diving appears necessary to reach

the critical velocity to create element C. The R5’s critical

velocity of 19.6G1.1 m sK1 (figure 4) is faster than the top

speed of 13 m sK1 at which the birds were observed to fly

in the wild (Stiles 1982), or the top speed of 15.1G0.48 m sK1 (nZ15) at which males are capable of flying in

a wind tunnel (Clark & Dudley in preparation). Many

other species of bird, such as snipes, nighthawks and other

hummingbirds, also perform dive displays while produ-

cing putative sonations. This suggests that diving from a

height may be a common strategy for achieving velocities

high enough to reach the feather’s critical velocity.

The Anna’s hummingbird can sing at the same

frequency as the dive sounds (figure 2a,b), raising the

question of why it has evolved a second mode of sound

production. The Anna’s hummingbird’s sister species, the

Costa’s hummingbird (Calypte costae; McGuire et al.

2007), also reportedly sings and produces its dive sounds

vocally, and these sounds are acoustically similar (Wells

et al. 1978). Its unusually shaped R5s are approximately

2 mm in width (the Anna’s is 4 mm), and the flag

hypothesis predicts that smaller widths will produce

higher-frequency sounds. The Costa’s dive sound has

higher frequency than the Anna’s dive sounds (Wells et al.

1978). These patterns suggest that the Costa’s dive sound

could be produced by the tail as well. If true, the

convergence in song and dive sounds may not be unique

to the Anna’s hummingbird, indicating that selection

favours similar acoustic features in both types of acoustic

signals. While sexual selection seems to be the most likely

cause of this convergence, the dive’s function is unclear.

Males perform dive to females, other males, other species

of birds and even to humans (Stiles 1982; but see Hurly

et al. 2001).

Proc. R. Soc. B (2008)

Non-vocal mechanisms, such as this tail feather

sonation, enhance the diversity of sounds birds can

produce. Small birds may be limited in their ability to

produce loud vocal sounds by the size of their syrinx

(Brackenbury 1979). The dive sound of the Anna’s

hummingbird is much louder than its song (figure 2a,b).

This suggests that switching to feather sonations has

allowed it to escape the intrinsic constraints on vocal

sound volume. In the bee hummingbird clade (which

includes the Anna’s hummingbird), many related species

perform dives (Banks & Johnson 1961; Stiles 1983; Clark

2006), have species-specific tail morphologies (Banks &

Johnson 1961; Wells et al. 1978) and make a diverse array

of sounds (Wells et al. 1978). This is likewise true for

snipes (Bahr 1907; Sutton 1981). We predict that in these

clades, dive behaviours and tail morphology have

coevolved to produce a diversity of mechanical sounds.

All procedures were approved by the UC Berkeley

Animal Care and Use Committee and performed under

the relevant government permits to film, capture and band

hummingbirds.

We are indebted to M. Koehl, B. Full, R. Dudley, M. Dennyand especially S. Patek for use of equipment; to N. Reeder,J. Derbridge, A. Haiman, S. Weinstein, A. Shultz, G. Byrnes,A. Varma and S. van Duin for assistance in the field; toS. Patek, L. Mahadevan, N. Fletcher, S. Sane, M. deVries,J. McGuire, the Dudley laboratory and members of the MVZfor advise and discussion; and to the USFWS, CADepartment of Fish and Game, Patuxent Bird BandingLab, California State Parks and East Bay Regional Parks forresearch and filming permits. Funding was provided by theMuseum of Vertebrate Zoology, and R. Dudley. C.J.C.performed the field experiments and wrote the majority ofthe paper as a part of a PhD thesis. T.J.F. designed andperformed the laboratory experiments as an undergraduatehonours thesis, and contributed substantially to fieldwork,data analysis and writing.

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